for azorean arthropods: evolution, diversity, rarity … · the target group are the arthropods,...

AÇOREANA, 2011, Suplemento 7: 93-123

PATTERNS OF COLONIZATION AND SPECIES DISTRIBUTION FOR AZOREAN ARTHROPODS: EVOLUTION, DIVERSITY,

RARITY AND EXTINCTION

Paulo A.V. Borges1, Clara Gaspar1, Ana M.C. Santos1, Sérvio Pontes Ribeiro1,2, Pedro Cardoso1,3, Kostas A. Triantis1,4 & Isabel R. Amorim1,5

1 Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Pico da Urze, 9700-042 Angra do Heroísmo, Portugal

e-mail: [email protected] Universidade Federal de Ouro Preto, Instituto de Ciências Exatas e Biológicas,

Lab. Ecologia Evolutiva de Herbívoros de Dossel/DEBIO, campus Morro do Cruzeiro, 35400-000, Ouro Preto, MG, Brasil

3Smithsonian Institution, National Museum of Natural History, Washington, DC, USA Department of Biology, Texas State University, San Marcos, TX, USA

4Biodiversity Research Group, Oxford University Centre for the Environment, South Parks Road, Oxford, OX1 3QY, UK

5School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, England, UK

ABSTRACTHere we address a list of questions based on long-term

ecological and biogeographical studies performed in the Azores, a remote volcanic oceanic archipelago composed by nine islands. The target group are the arthropods, and the main habitat the Laurisilva, the Azorean native forest. Diversification of Azorean arthropod species is affected by island age, area and isolation. However, results obtained for over a decade show that distinct groups are differently affected by these factors, which has lead to the extreme diverse distribution patterns currently observed. Spatial distribution of arthropods in each island may be interpreted as caused by a typical “mass effect”, with many species following a “source-sink” dynamics. Truly regionally rare species are those that are habitat specialists, many of them being threatened endemic species. Although various endemics persist as sink populations in human-made habitats (e.g., exotic forests), more than half of the original endemic forest arthropods may already have vanished or may eventually be driven to extinction in the future. Those species which have evolved in and are mainly found in native forests, have been dramatically affected by hitherto unrecognized levels of extinction debt, as a result of extensive destruction of native forest. We argue that immediate action to restore and expand native forest

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94 2011, Suplemento 7: 93-123A Ç O R E A N A

habitat is required to avoid a future of disastrous extinctions of a biologically unique fauna with an unique evolutionary history.

RESUMOCom base em estudos ecológicos e biogeográfi cos realizados nos

Açores (um arquipélago remoto composto por nove ilhas vulcânicas) durante muitos anos de uma forma continuada, apresentamos um conjunto de questões. O grupo alvo são os artrópodes e o principal habitat é a Laurissilva, a fl oresta nativa dos Açores. A diversifi cação das espécies de artrópodes dos Açores é afectada pela idade das ilhas, área das ilhas e seu isolamento. No entanto, os estudos que decorreram durante os últimos dez anos mostram que os vários tipos de grupos taxonómicos e ecológicos são afectados de forma diferente por estes factores, tendo como consequência padrões de distribuição espacial únicos. A distribuição espacial dos artrópodes em cada ilha é causada for “efeitos de massa”, muitas espécies possuindo dinâmicas “fonte-sumidouro”. As espécies verdadeiramente raras à escala regional são aquelas que são especialistas de um particular habitat, muitas delas sendo espécies endémicas ameaçadas. Embora várias espécies endémicas persistam com populações sumidouro em habitats criados pelo Homem (e.g. fl orestas exóticas), mais de metade das espécies especialistas da fl oresta nativa já estão extintas ou poderão extinguir-se no futuro. De facto, aquelas espécies que evoluíram e apenas são encontradas nas fl orestas nativas, foram afectadas de forma dramática como resultado da destruição alargada das fl orestas nativas dos Açores. Defendemos que a única forma de evitar a extinção de uma fauna única das fl orestas nativas dos Açores será através de medidas de restauro desta fl oresta.

INTRODUCTION

Charles Darwin and Alfred R. Wallace were both fasci-

nated by islands and the foundations of their evolutionary theory were mostly based on evidences obtained from iso-

lated oceanic islands like the Galápagos, Hawaii and Madeira. Their initial observations and conclusions were seminal for the formulation of comprehen-sive theorems and hypotheses on evolutionary mechanisms responsible for the maintenance


95BORGES ET AL.: PATTERNS IN AZOREAN ARTHROPODS

and increase of biodiversity following island colonization. Since then, islands have been regarded as natural laborato-ries for the study of evolution-ary, ecological and ecosystems processes (Vitousek et al., 1995; Wagner & Funk, 1995; Clarke & Grant, 1996; Thornton, 1996; Whittaker & Fernández-Palacios, 2007), due to their isolated character and their depauperated and disharmonic faunas and floras (Carlquist, 1974; Williamson, 1981; Whittaker & Fernández-Palacios, 2007). Changes in traits related to defences and flight, species radiation and endemism, as well as occupation of vacant niches, are just some examples of important fundamental con-cepts in Evolutionary Ecology developed as the result of data obtained from island biology studies (Whittaker & Fernández-Palacios, 2007). Not surprisingly, one of the most popular models in ecological literature is the “Theory of Island Biogeography” (MacArthur & Wilson, 1963, 1967), designed to explain patterns of species richness on islands, but with wider applications, namely in biodiversity, conservation and management (Rosenzweig, 2004).

Studies of island species and their natural histories have

become fundamental to the understanding of the evolution, biology and ecology of animals and plants. Good examples are the now classic works of Carlquist (1974) and Williamson (1981). Some important works were published about island archipelagos, like the Atlantic Islands (Berry, 1992; Hounsome, 1993; Biscoito, 1995; Ashmole & Ashmole, 2000; Fernández-Palacios & Martin Esquivel, 2002; Fernández-Palacios & Morici, 2004; Serrano et al., 2010), Hawaii (Wagner & Funk, 1995), Krakatau (Thornton & Rosengren, 1988; Thornton, 1996), Pacific Islands (Keast & Miller, 1996) and Pitcairn Islands (Benton & Spencer, 1995). Special publications on evolu-tion on islands (Clarke & Grant, 1996; Emerson, 2002; Gillespie & Roderick, 2002) and one unique on ecological function (Biological Diversity and Ecosystem Function on islands - Vitousek et al., 1995) have been published recently. More than describing unusual body adaptations, such as wingless birds and giant, arborescent herbs, recent studies emphasise how unique and distinct oceanic island ecosystems are. Special attention is given to how fragile



these ecosystems are and the need of urgent conservation measures.

Here we describe the results of a long-term ecological study on arthropods carried out in the Laurisilva, the native forest of the Azores, a remote volcanic oceanic archipelago. We address a list of questions arising from the results obtained from a number of studies performed in the last ten years.

AZOREAN NATURAL HISTORY AND BIODIVERSITY

Charles Darwin visited the Azores during the expedition of the Beagle (September 1836) (Keynes, 1988). Despite a dis-cussion on the mechanisms of dispersal, making reference to the neighbouring archipelago of Madeira, and some mention to arborescence of Erica azorica (only studied recently by Ribeiro et al., 2003), he made no significant comments about the arthropods of the Azores. Although the Azores is an isolated archipelago with a diverse geological history and a wide range of elevations, the relatively low endemic richness and the lack of remarkable adaptive radiation compared

with other archipelagos (e.g., Canary Islands) resulted in it receiving less attention (but see Wallace, 1876).

Crotch (1867) comments on the almost complete indifference of naturalists towards the Azores, noting, as an example, that while the English entomologist T.V. Wollaston intensively sampled in archipelagoes of Madeira, the Canaries and Cape Verde, he did little in the Azores. The historical lack of interest on Azorean arthropods can, in part, be explained by the lack of knowledge of the faunistic composition of many Azorean taxa until recently (but see Borges et al., 2005a, 2010a), but this trend is changing. Recently there has been an increasingly interest in the Azorean biota that is reflected in the raising number of publications on the biogeography, ecology, applied entomology, biospeleology and systematics of its arthropods (see details below). The present work shows the importance of evidence obtained from the Azores for the understanding of general island processes.

The current estimate of terres-trial species and/or subspecies in the Azores is 6,164 (about 6,112 species), of which 452 (411 spe-



cies) are endemic (Borges et al., 2010a) (see Table 1). Arthropods are the most diverse taxon with about 2,298 species and subspe-cies, 266 of which are endemic (Table 1; see also Borges et al., 2010a).

AZOREAN ARTHROPOD BIODIVERSITY: THE MAIN

QUESTIONS

Invertebrates are generally relegated to a secondary place in biodiversity conservation pro-grams and there are sociologi-cal, educational and scientific reasons for this (Cardoso et al., 2011a, b). One significant fac-tor is the lack of communication between scientists and stake-holders and overcoming this problem is essential for all ongo-ing arthropod research projects. Conservation of the Azorean natural biodiversity requires the elaboration of a global and in-tegrated strategy based on the knowledge of current species distributions and how of cur-rent land-use will impact future distributions (see e.g., Borges et al., 2008; Cardoso et al., 2009b; Meijer et al., 2011). Consequently it is crucial to understand how land overexploitation, increased tourist activities, displacement

of native species by exotic ones and climate change, may affect Azorean biodiversity and eco-system functioning. In the last ten years we have invested con-siderable effort to raise aware-ness about the importance of Azorean arthropod biodiversity relative to the total biodiversity of the Azores and of the Atlantic Biogeographic Region (see e.g., Borges et al., 2005a, 2008a, 2010a). Our ultimate goal is to ensure that the highly diverse endemic arthropods island bio-diversity conservation areas are protected, in the hopes that this will halt, and hopefully reverse, the general trend of biodiver-sity decline in the Azores (see Triantis et al., 2010a).

The BALA project (2000-2010; Biodiversity of Arthropods from the Laurisilva of the Azores) (see Borges et al., 2000, 2005b; Gaspar et al., 2008), that sur-veyed arthropods distribution in Azorean native forests, was an important step towards the inclusion of arthropod groups in biodiversity conservation plan-ning in the Azores. The system-atically collected data allowed inferences to be made about the biology, ecology, rarity and con-servation status of the different arthropod species. Transects



TABLE 1. Total and endemic terrestrial diversity (species and subspecies) of the main groups of the Kingdoms Fungi, Chromista, Protoctista, Plantae and Animalia in the Azores (more details in Borges et al., 2010a).

Kingdom and Phylum/Division Common name Total Endemic

FUNGI 1328 34Zygomycota (Fungi) Zygomycete fungi 2 0Ascomycota (Fungi) Sac fungi, Cup fungi 231 20

Ascomycota (Lichen) Lichen 775 10Basidiomycota (Fungi) Basidiomycete fungi 307 4

Basidiomycota (Lichen) Lichen 6 0Lichen (Fungi Imperfecti) Lichen 7 0

CHROMISTA 4 0Oomycota Water molds 4 0

PROTOCTISTA 575 7Bacillariophyta Diatoms 536 7

Amoebozoa Amoebae 39 0PLANTAE 1590 80

Bryophyta Bryophytes 480 7Anthocerotophyta Hornworts 5 0Marchantiophyta Liverworts 164 1

Bryophyta Mosses 311 6Tracheobionta Vascular Plants 1110 73

Lycopodiophyta Quillworts 7 1Pterydophyta Ferns 69 6

Pinophyta Gymnosperms 4 1Magnoliophyta Dicots and monocots 1030 65

ANIMALIA 2667 331Platyhelminthes Flatworms 31 0

Nematoda Roundworms 131 2Annelida Earthworms 22 0Mollusca Slugs and snails 114 49

Arthropoda Arthropods 2298 266Chordata (Vertebrata) Vertebrates 71 14

TOTAL 6164 452



(150 m x 5 m) were randomly placed within fragments of pro-tected native forest. The number of transects per forest fragment was set up using a logarithmic scale, assuming a species-area relationship (SAR) with a slope (z) of 0.35 in a log-log scale (i.e., a 10 fold area increase implies a duplication of the number of species): 2 transects were set up for 10 ha forest fragments, 4 transects for 100 ha frag-ments and 8 transects for 1,000 ha fragments. Consequently, higher sampling effort was ap-plied to larger protected native forest areas (i.e. “proportional sampling”), making it possible to capture not only “area per se effects” but also unveil patterns that could be prevalent in larger areas, such as, spatial beta diver-sity.

In this paper we compile and synthesize the results of recent research on the biodi-versity and ecology of Azorean arthropods, which were at least partly based on data obtained from long term projects (e.g., BALA, “Biodiversity of cave invertebrates”), and many oth-ers of shorter duration (e.g., Interfruta). During the last ten years several general questions were raised and several specific

goals (noted below) were pur-sued:

Inventory of Azorean arthropods and diversity hotspots

- list all arthropod taxa from the Azores (see Borges et al., 2005c, 2010b);

- describe new taxa (Blas & Borges, 1999; Ribes & Borges, 2001; Platia & Borges, 2002; Quartau & Borges, 2003; Borges et al., 2004, 2007; Borges & Wunderlich, 2008);

- examine the shape and charac-teristics of discovery curves in order to obtain a provi-sional picture of the taxo-nomic completeness of cur-rent inventories and an esti-mation of the amount of work still needed to attain taxo-nomic completeness (Lobo & Borges, 2010).

- identify hotspots of species diversity in the Azores (e.g. Borges et al., 2005b; Borges & Gabriel, 2009).

Ecological patterns of species distribution and abundance (i.e. rarity)

- test if the He & Gaston (2003) a b u n d a n c e – va r i a n c e – o c -cupancy model accurately predicts species distribution across different spatial scales



and whether endemic, na-tive (non-endemic) and intro-duced species occupy differ-ent parts of the abundance– variance–occupancy space (Gaston et al., 2006);

- assess patterns of distribu-tion and species richness of canopy phytophagous in-sect among islands and host plants (see Ribeiro et al., 2005; Santos et al., 2005);

- describe patterns of rarity in one well-sampled island, i.e., Terceira, identifying types of local pseudo-rare species (Borges et al., 2008);

- explore patterns of diversity, abundance and distribution of different taxonomic, colo-nization and trophic groups of arthropods in Azorean na-tive forests at different strata and sites (Gaspar et al., 2008);

- test the “resource concentra-tion hypothesis”, that pre-dicts there is a positive rela-tionship between the density of phytophagous insects or predator arthropods and the spatial distribution/abun-dance of host plants (Ribeiro & Borges, 2010);

- test if more abundant and widespread plant species are those that support popula-tions of the rarest regional

arthropod species (Ribeiro & Borges, 2010);

Evaluate the role of environmental variables

- examine how a variety of biotic, abiotic and anthropogenic fac-tors infl uence endemic and in-troduced arthropod richness on an oceanic island (Terceira) (Santos et al., 2005; Borges et al., 2006);

- evaluate the degree to which environmental suitability as-sessed with presence/absence models account for abun-dance estimates (Jimenez-Valverde et al., 2009);

Effects of scale and sampling on species richness, beta diversity and density

- analyze the effect of varia-tion in the size of sampling units on species richness es-timations, and evaluate the accuracy of the predictions obtained with various estima-tors presently available when different strategies are used to group the same dataset into different sized samples (Hortal et al., 2006);

- assess how differently beta diversity measures for in-cidence data and pairwise comparisons behave with re-



gard to varying degrees of sampling effort, and recom-mend diversity measures that are relatively robust to un-dersampling (Cardoso et al., 2009a);

- test the hypothesis that “host-habitat area” affects the fol-lowing insect density esti-mates: mean number per tree canopy or reserve transects (Ribeiro & Borges, 2010).

Effect of disturbance in ecological communities

- understand how several taxo-nomic and ecological attri-butes of arthropod communi-ties vary with respect to dif-ferent levels of disturbance as well as assessing to what extent potential disturbance factors are influencing site integrity (Santos et al., 2005; Cardoso et al., 2007);

Biogeography of Azorean arthropods- investigate some biodiversity

patterns relating to spider distribution between islands, habitats, colonization status and biogeographical origin (Borges & Wunderlich, 2008);

- study the factors promot-ing diversification of several Azorean arthropod groups (Borges & Hortal 2009) and

extending this to the rest of Macaronesia (Cardoso et al., 2010a; Triantis et al., 2010b);

- identify the biogeographi-cal factors underlying spi-der species richness in the Macaronesian region and assessing the importance of species extinctions in shaping current diversity (Cardoso et al., 2010a);

- investigate whether there is a significant gain in in-formation if one uses non-parametric richness esti-mators to build SAR models with standardized surveys data, rather than using the observed number of species (Sobs) (Borges et al., 2009);

- investigate if species-area relationships from entire ar-chipelagos are congruent with those of their constituent islands (Santos et al., 2010).

Surrogacy patterns in arthropods- evaluate the effectiveness of

arthropods as predictors of diversity for a wide range of taxonomic and non-taxo-nomic groups, for multiple measures of biodiversity and for different spatial scales (Gaspar et al., 2010);

- evaluate the effectiveness of cave-adapted arthropods as



predictors of diversity of rare bryophytes in cave entrances and the diversity of bacteria in cave mats.

Conservation of Azorean arthropods- examine the relative value of 19

forest fragments in seven of the Azorean islands to improve the conservation of Azorean soil epigean arthropod biodi-versity (Borges et al., 2005b; Gaspar et al., 2011);

- investigate the relationships between endemic and intro-duced arthropod richness, to assess whether areas with high levels of endemic spe-cies richness deter invasions (Borges et al., 2006);

- investigate the relevance of current human-made habitats (e.g. exotic forest; agroeco-systems) for the protection of rare species (see Cardoso et al., 2009b, 2010b; Meijer et al., 2011);

- test nestedness patterns of en-demic, native and introduced species (Cardoso et al., 2010b);

- quantify the magnitude and taxonomic distribution of ex-tinction debt in the Azores as an important step for effec-tive conservation planning (Triantis et al., 2010a);

- list the 100 highest man-

agement priority taxa in Macaronesia and in the Azores, the so-called Top 100 (Cardoso et al., 2008; Martín et al., 2010).

- genetic characterization of populations of endemic species to investigate their uniqueness and examine how this informa-tion could help in the prioriti-zation of conservation eff orts.

WHAT HAVE WE LEARNED SO FAR?

Inventory of Azorean arthropods and diversity hotspotsThe knowledge base of

Azorean arthropod biodiversity is not uniform, and many groups have not been adequate-ly sampled. Furthermore, many groups have not received appro-priate taxonomic revision, due to little traditional taxonomic research being carried out in the last decade, and the lack of taxonomists familiar with the Azorean fauna (Amorim, 2005; Borges et al., 2005a; Lobo & Borges, 2010). As with any other biome, solving this problem is not simple since, for exam-ple, traditional taxonomic work has been neglected in the last decades in Europe (see Boero, 2010). The most relevant effort



to rectify the lack of taxonomic expertise preventing advance in biodiversity research was the establishment of the “Azorean Biodiversity Group” (http://cita.angra.uac.pt/biodiversidade/), that, among other things, is sup-porting research on classical (as well as molecular) taxonomy and ecology of arthropods of the Azores. Moreover, the web site “Azorean Biodiversity Portal” (http://www.azoresbioportal.angra.uac.pt/) (see Borges et al., 2010c) allows everyone to ac-cess updated information on Azorean biodiversity. As a di-rect outcome of this online data-base many national and interna-tional taxonomists have shown a growing interest in Azorean bio-diversity and many new collabo- rations have been established, including taxonomic revisions (see Borges et al., 2010b) and additional field work to collect specimens.

The results obtained during the BALA project (see above) showed that some forest reserves are clearly more diverse than others, both in terms of alpha and gamma diversities. The effect of forest fragmentation has not been studied in detail (see future work below), but the data obtained suggests that small

fragments play a much more important role than previously thought (see Borges et al., 2005b; Borges & Gabriel, 2009). For instance, based both on the presence of unique species and high species richness, the Pico Alto region in the archipelago´s oldest island, Santa Maria, is a hotspot of biodiversity (Borges et al., 2005b; Borges & Gabriel, 2009). Over 57 endemic arthropod species are known from Pico Alto (Santa Maria Isl.), i.e. 21% of the Azorean endemic arthropods occurring in an area representing <0.25% of Azorean native forests. Other relevant areas occur on the islands of São Miguel (Pico da Vara), Terceira (Terra Brava, Caldeira da Serra de Santa Bárbara), São Jorge (Topo), Pico (Caveiro, Mistério da Prainha) and Flores (Morro Alto and Pico da Sé) (see Borges & Gabriel, 2009; online at http://www.azoresbioportal.angra.uac.pt/files/publicacoes_Brochura BIODIVERSIDADE AORES vFINAL.pdf).

Results obtained from oth-er studies, such as the survey of subterranean invertebrates (1999-2005) revealed the poor stage of knowledge on the Azorean cave invertebrates. For instance, the number of cave



Trechus listed for the islands in-creased from 4 to 7, plus an epi-gean species in the same genus (Borges et al., 2004; Amorim, 2005; Borges et al., 2007).

Ecological patterns of species dis-tribution and abundance (i.e. rarity)The data for diverse species

assemblages at different spatial scales, regardless of species status, can be well described by an abundance-variance-occupancy model (Gaston et al., 2006). Most importantly, we observed that outliers include restricted specialized forest endemic species (e.g. Trechus terrabravensis and Cedrorum azoricus azoricus) that only occupy pristine native forest sites where they are quite abundant (Gaston et al., 2006).

We have found that free-living herbivores insect in the canopies of Azorean native forests are mainly generalists, as expected for a relatively young and isolated volcanic archipelago (Ribeiro et al., 2005). Interestingly, the proportion of rare species is higher for herbivores insects than for predatory arthropods (Borges et al., 2008). Ribeiro & Borges (2010) also showed that there is

a clear dominance of generalist species in canopies of Azorean trees and shrubs, which holds also true for the overall spider and chewing insect communities in Terceira island (Borges et al., 2008). The observation of a widespread distribution of spiders on tree canopies in the native forest could be explained by their high dispersal ability and generalist feeding habits (Borges & Wunderlich, 2008). Consequently, the abundance of herbivorous insects seems to be strongly affected by the occurrence and population densities of spider species. One particular plant species, Erica azorica, has greater than expected herbivore densities per crown, possibly as it represents enemy free/predictable space (Ribeiro & Borges, 2010). In the case of agricultural habitats, we found that both abundance and species richness of predatory groups inhabiting the canopy of different fruit trees (apple, orange, and peach trees) are negatively correlated with canopy volume, and positively correlated with tree density. On the other hand, herbivore species, especially sucking insect species, show the opposite trend (Santos et al., 2005).



In terms of rarity, four important types were detected in the Azores (see Borges et al., 2008; Ribeiro & Borges, 2010): 1) dense and intermediately dense species; 2) truly rare species, which are rare on any host species and with very low population densities regionally; 3) pseudo-rare species found in small numbers on a specific host tree, which are dense on neighbouring tree species, i.e. host-tourists; 4) pseudo-rare species found in small numbers on any tree species that are common in other habitats on the island, i.e., habitat-tourists.

Truly rare and specialist species should also be favoured by the presence of large quantities of resources, and although large tree species have similar numbers of rare species, most of these species are truly rare on Juniperus brevifolia, Laurus azorica and Erica azorica (see Ribeiro & Borges, 2010). Therefore, the high frequency of E. azorica and J. brevifolia populations throughout the Azorean native forest fragments creates the opportunity for the survival of rare insect and spider species populations on these hosts (Ribeiro & Borges, 2010).

Other surveys focused on

arthropods from very specific habitats typical of volcanic islands such as the Azores - lava tubes and volcanic pits - revealed that cave adapted species rarity vary as a function of cave abundance and the number that have actually been sampled (see Amorim, 2005). For the most studied Azorean cave beetle species, (in the genus Trechus) some are found at high densities at many sites (e.g., T. picoensis from Pico Isl. occurs in 9 caves and 134 specimens have been collected so far from the Torres lava tube), while others are only found at one site and despite the amount of sampling efforts involved only a few specimens have been collected (e.g., only 2 individuals of T. jorgensis are known from Bocas do Fogo pit in São Jorge Isl.).

Evaluate the role of environmental variablesWe have shown for the soil

arthropod fauna of native for-est in Terceira Island that abiotic (climatic and geomorphologi-cal) variables provided a better explanation for the variation in endemic species richness than anthropogenic ones, whereas the inverse was observed with respect to introduced species



richness (see Borges et al., 2006). Concerning the abundance of species, Jimenez-Valverde et al., (2009) observed that Azorean ar-thropod species are highly influ-enced by land-use variables, in such a way that the climate fac-tors lose relevance and the cli-matic suitability may be diluted in predicting local abundance of species. However, in their analysis of the arthropod com-munities associated with fruit orchards, Santos et al., (2005) found a strong influence of both climatic and anthropogenic vari-ables on the abundance and di-versity of different functional guilds.

Effects of scale and sampling in species richness, beta diversity and densityArthropod data from BALA´s

standardized sampling proto-col was used to evaluate the ef-fects of scale (across sites, for-est fragments and islands) and sampling in species richness, beta diversity and density (see Hortal et al., 2006; Cardoso et al., 2009a; Ribeiro & Borges, 2010). Several estimators (ACE, Chao1, Jackknife1 and 2 and Bootstrap) provided consistent estimations of species richness, regardless of sample grain size. In addition

several nonparametric estima-tors presented certain insensi-tivity to how samples are aggre-gated (Hortal et al., 2006).

Cardoso et al., (2009a) dem-onstrated that beta diversity values are close to the real val-ues, when communities being compared approach sampling completeness. However, the β-2 index from Harrison et al., (1992) should be used as the most con-sistent measure in cases in which the sampling completeness de-gree of a dataset is unknown.

In general, the three structural-ly most complex and abundant plant “host islands”, i.e., E. azorica, J. brevifolia and L. azorica, accumulated the highest proportion of regionally rare arthropod species, corroborating the “host as an island hypothesis” (Ribeiro & Borges, 2010).

Effect of disturbance in ecological communitiesIn broad terms current frag-

ments of Azorean native forest are not uniform in their conser-vation status. In fact, Cardoso et al. (2007) clearly demon- strated that when using an Index of Biotic Integrity (IBI) adapted to the epigean arthropods of the Azorean native forests, many fragments of native forest would



be considered highly disturbed. More importantly, these au-thors showed that most species thrived in highly disturbed sites are of limited importance for conservation efforts, and that the percentage of endemic spe-cies is significantly higher in pristine than in degraded sites.

Biogeography of Azorean arthropodsBorges & Brown (1999)

showed that island geological age was an important variable explaining Azorean endemic arthropods species richness. Recently, there has been in-creased interest in the determin-ing the importance of geologi-cal age and other geographical variables to explain patterns of island diversity in Macaronesia (e.g. Whittaker et al., 2008, 2009; Borges & Hortal, 2009; Borges et al., 2009; Cardoso et al., 2010a; Triantis et al., 2010b).

In most of these studies the main observation was that a combination of islands’ area and geological age are enough to provide a basic explanation for the diversity of endemic ar-thropods in the Azores, in spite of some differences between taxonomic or ecological groups and the additional role of is-land relative isolation (Borges &

Hortal, 2009; but see Cardoso et al., 2010a). The main conclusion was that due to the recent age of the archipelago (see Borges & Hortal, 2009; Triantis et al., 2010b) a simple area-age model (AT) is adequate for the Azorean fauna, and not the more com-plex area-age-age2 (ATT2) first-ly proposed by Whittaker et al. (2008, 2009) within the context of The General Dynamic Model of Oceanic Island Biogeography (GDM). In fact, when testing the GDM, Borges & Hortal (2009) showed that: i) cave species appear to have evolved quite quickly, producing a number of species during the initial stages of island development, when cave systems formed by lava tubes and volcanic pits were abundant and pristine prior to natural collapsing of structures; ii) taxa with low dispersal abil-ity, particularly beetles, showed strong negative relationships with the distance to Santa Maria, the oldest island and reservoir of lineages either coming from the mainland or remaining from the older archipelago composed of Santa Maria and the Northeast part of São Miguel; iii) the diver-sity of evolutionary responses in different organisms is so var-ied that no general model, like



the one proposed by Whittaker and colleagues (Whittaker et al., 2008, 2009) is able to predict the patterns and processes of diver-sification.

Spiders apparently follow a different pattern from the one observed for most arthropod groups. Analyzing the biogeo-graphical factors underlying spider species richness in the Macaronesian region Cardoso et al. (2010a) showed that for the Azores, island area and the proportion of remaining natural forest were the best predictors of species richness. The effect of island age on species richness, if important in diversification processes, has nowadays been masked by the effect of native habitat destruction. Triantis et al. (2010b) found that the AT model was the most parsimoni-ous for explaining diversity pat-terns of indigenous, endemic, single island endemic and pro-portion of single island endemic beetles and arthropods in the Azores, corroborating the re-sults of Borges & Hortal (2009).

Santos et al. (2010) observed that archipelagos follow the same island species–area rela-tionships (ISAR) as their consti-tuent islands, which means that the Macaronesian archipelagos

could be studied as four data points when testing the relation-ship between species richness and area. Borges et al. (2009) found that if data comes from standardized surveys (as is the case of BALA data), the slope and goodness of fit for species area relationships obtained with estimated values (using non-parametric estimators; see also Hortal et al., 2006) were not sig-nificantly different from those obtained from observed species richness.

Molecular data generated for a few Azorean endemic arthro-pods groups (the beetles Trechus and Tarphius, and the butter-fly Hipparchia) and their neigh-boring insular and continental congeneric species reveal that the Azorean taxa form mono-phyletic clades (Fujaco et al., 2003; Amorim, 2005). This sup-ports single colonization events of the Azores, as expected for such remote oceanic island. If true, then the diversification currently observed within these groups would be the result of in-tra archipelago speciation from single ancestors, as opposed of multiple arrivals of distinct lineages (Amorim et al., subm.). Nevertheless, the possibility that multiple colonization events oc-



curred but have gone extinct cannot be completely dismissed.

Surrogacy patterns in arthropodsGaspar et al. (2010) evaluated

the effectiveness of taxonomic, colonization and trophic groups of arthropods from native forests of the Azores archipelago as sur-rogates of the diversity of other arthropod groups. The results indicated that spiders (Araneae) and true bugs (Hemiptera) may be more promising surrogates of arthropod diversity for the Azorean native forests at the transect, fragment and island scales (Gaspar et al., 2010). As spiders are easy to identify, abundant in both terrestrially and within tree canopies (Borges & Wunderlich, 2008; Borges et al., 2008; Gaspar et al., 2008) and probably good indicators of futures trends for other taxa (Cardoso et al., 2010a), we sug-gest the use of this group for fu-ture rapid monitoring studies in Azorean forests.

Conservation of Azorean arthropodsHuman activities and inva-

sive species are among the most important factors impacting Azorean arthropod communi-ties (Godman, 1870; Borges et al., 2006, 2008). The number of

described species known from the Azores is continuously ris-ing (Borges et al., 2010a), but a great proportion are recently introduced ones, that tend to exhibit lower densities, less spa-tial density variance, and oc-cupy fewer sites than native and endemic species (Gaston et al., 2006). On Terceira island, non-indigenous species are mainly limited to those sites under an-thropogenic influence located mainly on low to medium alti-tude areas or, when in high-alti-tude forests, in marginal areas of the few forest remnants (Borges et al., 2006). For example, the protection of forest specialists, like the ground-beetles Trechus terrabravensis and Cedrorum azo-ricus azoricus (see Gaston et al., 2006) requires the management of invasive species, to avoid them entering the pristine native forest sites, such as those found in Serra de Santa Bárbara (see also Borges et al., 2006; Cardoso et al., 2007).

The impacts of land use changes are severe (Borges et al., 2008; Cardoso et al., 2009) and many Azorean endemic forest dependent species are on the edge of extinction (Triantis et al., 2010a). Despite the fact that un-managed exotic forests are pro-



viding alternative habitat suit-able for some endemic species (forest specialist arthropods, particularly saproxylic beetles from S. Maria Island; Meijer et al., 2011), most endemic for-est specialist arthropods are restricted to native forests and only have sink populations in semi-natural grasslands or ex-otic forests (Borges et al., 2008; Cardoso et al., 2009; Triantis et al., 2010a).

Endemic and introduced species were all found to be highly nested in habitats of Terceira Island. Indeed, native forests and intensively man-aged pastures seem to be the main drivers of species compo-sition at any site, having most-ly endemic and introduced species, respectively (Cardoso et al., 2010b). This result im-plies that there is a predictable pattern of species loss and gain from natural forests to exotic forests, semi-natural pastures and finally intensively man-aged pastures, as suggested by the nestedness analysis (Cardoso et al., 2009b; 2010b). The roles of selective extinction (see also Triantis et al., 2010a), as is exemplified by a gradi-ent of disturbance (Cardoso et al., 2007), and habitat change

could explain the nested pat-tern for endemics.

Interestingly, hardly any ex-otic insect or spider were able to colonize the native forest can-opy habitat (Borges et al., 2008; Borges & Wunderlich, 2008), so are not widespread in all the Azorean habitats. For instance, the Azorean Laurisilva seems that has not yet been colonized by any of the invasive ant spe-cies found adjacently to hu-man constructions. Spiders are the most abundant terrestrial predators in the Azores (Borges & Wunderlich, 2008; see also Gaspar et al., 2008), particular-ly in forests, and may serve as early indicators for future disap-pearance patterns of other insu-lar taxa (Cardoso et al., 2010a).

The most disturbed study sites in the Azores were found on the islands of Faial (Cabeço do Fogo), Flores (Caldeiras Funda, Rasa), Pico (Lagoa do Caiado), São Jorge (Pico Pinheiro), São Miguel (Atalhada, Graminhais, Pico da Vara), Santa Maria (Pico Alto) and Terceira (Algar do Carvão, Matela, Pico do Galhardo), while the pristine areas were on Terceira (Terra Brava, Biscoito da Ferraria, Caldeira da Serra de Santa Bárbara), Pico (Caveiro, Mistério da Prainha) and Flores



(Morro Alto, Pico da Sé) islands (Cardoso et al., 2007; Gaspar et al., 2011).

Invasive plant species are the most important drivers in terms of ecological and ecosystem change in the Azores (Borges et al., 2010d) and the spread of spe-cies like Hedychium gardneranum, Hydrangea macrophylla, Rubus ulmifolius, Pittosporum undula-tum, Clethra arborea (see Silva & Smith, 2006; Hortal et al., 2010) is of great concern. Areas of high conservation value due to the presence of single island endemics, such as Pico Alto on Santa Maria and Pico da Vara on São Miguel, are now heav-ily disturbed by invasive plants. Human driven ecosystem distur-bances have to be minimized and special measures by the Azorean Government are already being applied for the control of inva-sive plants in several islands. The ongoing projects in Pico da Vara (S. Miguel) to manage areas of special importance for birds are good examples of active con-servation in the Azores (e.g. Ceia et al., 2009; Heleno et al., 2009).

A list of Azorean threatened taxa, based on both protec-tion priority and management feasibility, has been drawn up (Cardoso et al., 2008; Martín et

al., 2010). Arthropods represent 17 species of the 100 most impor-tant Macaronesian taxa (Martín et al., 2010) and 24 of the 100 most important in the Azores (Cardoso et al., 2008). This list will be used to determine those new species to be included in the revision of the NATURA 2000 list of Azorean priority spe-cies for conservation (Paulino Costa, pers. comm.). This will be an important step towards the inclusion of arthropods in conservation initiatives for the Azorean archipelago, includ-ing several new areas based on the occurrence of unique arthro-pod species (e.g. Atalhada in São Miguel; Pico Alto in Santa Maria; Fontinhas in Terceira) (see Gaspar et al., 2011).

Future work in the conservation of Azorean biodiversity

The study of arthropod ecol-ogy in the Azores has proven to be a valuable tool for designing biodiversity conservation plans in the archipelago. However, any hope for a successful man-agement and conservation pro-gram of endemic fauna and flora must meet local economic interests. Local people, with di-rect interest in the use of land for agriculture have a higher



impact on the sustainability of the Azorean habitats than policy makers, managers and conserva-tionists altogether. Several ini-tiatives, resulting from outcomes of the BALA project, have been undertaken through organized seminars and meetings as well as brochures and books (Borges & Gabriel, 2009; Cardoso et al., 2009c) in recent years increasing public understanding of why value arthropod biodiversity and thus to protect their habi-tats. The information on arthro-pod diversity and distribution provided by the BALA project and parallel studies is being used by the regional government to define and give legal status to the designated areas for protec-tion. The next steps would be to establish management plans for the areas, including the estab-lishment of periodic diversity monitoring plans for these zones to determine the effectiveness of the conservation strategies ad-opted to date. The management and monitoring plans should include: i) the identification of specific threats to the protected areas, ii) the definition of practi-cal measures to minimize these threats, and iii) the selection of specific groups of organisms and sampling methods that can

be used to periodically monitor the overall diversity of the areas.

FUTURE RESEARCH AND CONCLUDING REMARKS

The islands of the Azores have undergone dramatic changes in land-use and their biodiversity is now under serious threat (see Borges et al., 2008). With the current knowledge on Azorean arthropod biodiversity it is now possible to address more com-plex issues, such as being able to:1) predict species extinctions

using the available informa-tion of species abundance on Azorean islands (see also Triantis et al., 2010a) and com-pare data obtained in 1999-2000 with new data that was collected in 2010 (FCT Project PTDC/BIA-BEC/100182/2008 – “Predicting extinctions on islands: a multi-scale assess-ment);

2) evaluate the extent and the mechanisms through which fragmentation of natural habitats affects species com-munities. To do this, we will build a relevant framework to evaluate and compare habi-tat size effects on the species richness of native versus ex-



otic free-living herbivore in-sects and predatory spiders. We anticipate that these re-sults will advance in species–area relationship modelling techniques, that are crucial for both theoretical and con-servation applications in the Azores (see a recent appli-cation in Guilhaumon et al., 2008);

3) the study of species-environ-ment relationships, as islands are especially good places to address these questions;

4) identify evolutionary signifi-cant units for conservation by generating mitochondrial and nuclear molecular datasets of several arthropod endemic species (e.g., FCT - PTDC/BIA-BEC/104571/2008 project – “What can the Macaronesian islands teach us about specia-tion? A case study of Tarphius beetles and Hipparchia butter-flies”).Further studies, using dif-

ferent sampling techniques, should be carried out to im-prove our knowledge of the di-versity and distribution of less known groups of arthropods, such as Hymenoptera, Diptera, Collembola and Acari, these less known groups of arthropods are diverse and abundant and

should play important function-al roles in native communities.

Time scale, whether it is hours, days, months or years, has seldom been explored in the previous projects, despite the fact it will also influence the way diversity and distribution of arthropods is perceived, and hence, may provide additional information that is important for conservation planning. A study is currently exploring spi-der diversity in a native forest fragment at different hours of the day (Cardoso, unpublished data). Furthermore, a com-parison of data from 2000 with those from 2010 (FCT Project PTDC/BIA-BEC/100182/2008 – “Predicting extinctions on is-lands: a multi-scale assessment; Triantis et al., 2010a) will also offer valuable insights on the ef-fect of time scale on the diversity and distribution of arthropods in the Azores.

The patterns and causes of ar-thropod rarity in Azorean native forests should continue to be ex-plored in detail to distinguish between arthropod species that are truly rare from those that are rare at a given time, as this has major implications for the defi-nition of the most effective con-servation strategies.



ACKNOWLEDGEMENTS

We are grateful to all of the researchers that collaborated in the field and laboratory dur-ing BALA and other recent pro-jects: Álvaro Vitorino, Anabela Arraiol, Ana Rodrigues, Artur Serrano, Carlos Aguiar, Catarina Melo, Francisco Dinis, Genage André, Emanuel Barcelos, Fernando Pereira, Hugo Mas, João Amaral, João Moniz, Joaquín Hortal, Lara Dinis, Paula Gonçalves, Sandra Jarroca and Luís Vieira. The Forest Services provided local support on each island. Acknowledgments are due to all of the taxonomists who assisted in the identifi-cation of the morphotypes: Andrew Polaszek, António Bivar Sousa, Artur Serrano, Arturo Baz, Célia Mateus, Fernando Ilharco, Henrik Enghoff, John Noyes, Jordi Ribes, José A. Quartau, Jörg Wunderlich, Kees van Achterberg, Maria dos Anjos Ferreira, Mário Boieiro, Ole Karsholt , Richard Strassen, Volker Manhert and Virgílio Vieira. Field work for BALA project was also funded by the Azorean Direcção Regional dos Recursos Florestais (Proj. 17.01-080203). More recent projects were also relevant to the results

summarized in this manuscript: “Identification of genetically distinct populations of Azorean endemic arthropod species for biodiversity conservation in the archipelago” (Ref: Direcção Regional da Ciência e Tecnologia - DRCT M2.1.2/I/017/2007), “Consequences of land-use change on Azorean fauna and flora - the 2010 Target” (Ref: DRCT M.2.1.2/I/003/2008), the EU projects INTERREGIII B “ATLÂNTICO” (2004-2006) and BIONATURA (2006-2008). PAVB is currently being supported by the FCT project PTDC/BIA-BEC/100182/2008 – “Predicting extinctions on islands: a multi-scale assessment” and FCT pro-ject PTDC/BIA-BEC/104571/2008 - “ What can the Macaronesian islands teach us about specia-tion? A case study of Tarphius beetles and Hipparchia butter-flies”. CG is supported by the DRCT BPD 1.1.2/FRCT with the project: “Agriculture, habitat fragmentation, indicator species and conservation of endemic fauna and flora in the Azores – the 2010 Target”. AMCS was supported by the grant SFRH/BD/21496/2005. SPR is grant-ed by the Brazilian Council of Science and Technology, CNPq. PC is supported by the grant



FCT- SFRH/BPD/40688/2007. KT is supported by the grant FCT – SFRH/BPD/44306/2008. IRA is supported by a grant from FGF (PTDC/BIA-BEC/104571/2008).

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